Browse > Article

Membrane Topology of Helix 0 of the Epsin N-terminal Homology Domain  

Kweon, Dae-Hyuk (Department of Genetic Engineering, Faculty of Life Science and Technology, Sungkyunkwan University)
Shin, Yeon-Kyun (Department of Biochemistry, Biophysics and Molecular Biology, Iowa State University)
Shin, Jae Yoon (Department of Genetic Engineering, Faculty of Life Science and Technology, Sungkyunkwan University)
Lee, Jong-Hwa (School of Bioresource Sciences, Andong National University)
Lee, Jung-Bok (School of Bioresource Sciences, Andong National University)
Seo, Jin-Ho (Department of Agricultural Biotechnology, Seoul National University)
Kim, Yong Sung (Department of Biotechnology, Ajou University)
Publication Information
Molecules and Cells / v.21, no.3, 2006 , pp. 428-435 More about this Journal
Abstract
Specific interaction of the epsin N-terminal homology(ENTH) domain with the plasma membrane appears to bridge other related proteins to the specific regions of the membrane that are invaginated to form endocytic vesicles. An additional $\alpha$-helix, referred to as helix 0 (H0), is formed in the presence of the soluble ligand inositol-1,4,5-trisphosphate [$Ins(1,4,5)P_3$] at the N terminus of the ENTH domain (amino acid residues 3-15). The ENTH domain alone and full-length epsin cause tubulation of liposomes made of brain lipids. Thus, it is believed that H0 is membrane-inserted when it is coordinated with the phospholipid phosphatidylinositol-4,5-bisphosphate [$PtdIns(4,5)P_2$], resulting in membrane deformation as well as recruitment of accessory factors to the membrane. However, formation of H0 in a real biological membrane has not been demonstrated. In the present study, the membrane structure of H0 was determined by measurement of electron paramagnetic resonance (EPR) nitroxide accessibility. H0 was located at the phosphate head-group region of the membrane. Moreover, EPR line-shape analysis indicated that no pre-formed H0-like structure were present on normal acidic membranes. $PtdIns(4,5)P_2$ was necessary and sufficient for interaction of the H0 region with the membrane. H0 was stable only in the membrane. In conclusion, the H0 region of the ENTH domain has an intrinsic ability to form H0 in a $PtdIns(4,5)P_2$-containing membrane, perhaps functioning as a sensor of membrane patches enriched with $PtdIns(4,5)P_2$ that will initiate curvature to form endocytic vesicles.
Keywords
Endocytosis; ENTH; EPR; Epsin; Helix 0; Membrane Binding; Phosphatidylinositol-4,5-Bisphosphate;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 7  (Related Records In Web of Science)
연도 인용수 순위
1 Brasseur, R., Cornet, B., Burny, A., Vandenbranden, M., and Ruysschaert, J. M. (1988) Mode of insertion into a lipid membrane of the N-terminal HIV gp41 peptide segment. AIDS Res. Hum. Retroviruses 4, 83-90   DOI   ScienceOn
2 Brodsky, F. M., Chen, C. Y., Knuehl, C., Towler, M. C., and Wakeham, D. E. (2001) Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17, 517-568   DOI   ScienceOn
3 De Camilli, P., Chen, H., Hyman, J., Panepucci, E., Bateman, A., et al. (2002) The ENTH domain. FEBS Lett. 513, 11-18   DOI   ScienceOn
4 Epand, R. M., Hui, S. W., Argan, C., Gillespie, L. L., and Shore, G. C. (1986) Structural analysis and amphiphilic properties of a chemically synthesized mitochondrial signal peptide. J. Biol. Chem. 261, 10017-10020
5 Itoh, T., Koshiba, S., Kigawa, T., Kikuchi, A., Yokoyama, S., et al. (2001) Role of the ENTH domain in phosphatidylinositol- 4,5-bisphosphate binding and endocytosis. Science 291, 1047- 1051   DOI
6 Kweon, D. H., Kim, C. S., and Shin, Y. K. (2003) Regulation of neuronal SNARE assembly by the membrane. Nat. Struct. Biol. 10, 440-447   DOI   ScienceOn
7 Legendre-Guillemin, V., Wasiak, S., Hussain, N. K., Angers, A., and McPherson, P. S. (2004) ENTH/ANTH proteins and clathrin-mediated membrane budding. J. Cell Sci. 117, 9-18   DOI   ScienceOn
8 Schmidt, A. A. (2002) Membrane transport: the making of a vesicle. Nature 419, 347-349   DOI
9 Stahelin, R. V., Long, F., Peter, B. J., Murray, D., De Camilli, P., et al. (2003) Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin Nterminal homology (ENTH) domains. J. Biol. Chem. 278, 28993-28999   DOI   ScienceOn
10 Yu, Y. G., Thorgeirsson, T. E., and Shin, Y. K. (1994) Topology of an amphiphilic mitochondrial signal sequence in the membrane-inserted state: a spin labeling study. Biochemistry 33, 14221-14226   DOI   ScienceOn
11 Brett, T. J., Traub, L. M., and Fremont, D. H. (2002) Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure (Camb). 10, 797-809   DOI   ScienceOn
12 Higgins, M. K. and McMahon, H. T. (2002) Snap-shots of clathrin-mediated endocytosis. Trends Biochem. Sci. 27, 257- 263   DOI
13 Macosko, J. C., Kim, C. H., and Shin, Y. K. (1997) The membrane topology of the fusion peptide region of influenza hemagglutinin determined by spin-labeling EPR. J. Mol. Biol. 267, 1139-1148   DOI   ScienceOn
14 Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., et al. (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366   DOI   ScienceOn
15 Rabenstein, M. and Shin, Y. K. (1995) A peptide from the heptad repeat of human immunodeficiency virus gp41 shows both membrane binding and coiled-coil formation. Biochemistry 34, 13390-13397   DOI   ScienceOn
16 McHaourab, H. S., Kalai, T., Hideg, K., and Hubbell, W. L. (1999) Motion of spin-labeled side chains in T4 lysozyme: effect of side chain structure. Biochemistry 38, 2947-2955   DOI   ScienceOn
17 Han, X. and Tamm, L. K. (2000) A host-guest system to study structure-function relationships of membrane fusion peptides. Proc. Natl. Acad. Sci. USA 97, 13097-13102   DOI   ScienceOn
18 Columbus, L. and Hubbell, W. L. (2002) A new spin on protein dynamics. Trends Biochem. Sci. 27, 288-295   DOI
19 Kinuta, M., Yamada, H., Abe, T., Watanabe, M., Li, S. A., et al. (2002). Phosphatidylinositol 4,5-bisphosphate stimulates vesicle formation from liposomes by brain cytosol. Proc. Natl. Acad. Sci. USA 99, 2842-2847   DOI   ScienceOn
20 Altenbach, C., Marti, T., Khorana, H. G., and Hubbell, W. L. (1990) Transmembrane protein structure: spin labeling of bacteriorhodopsin mutants. Science 248, 1088-1092   DOI
21 Nossal, R. and Zimmerberg, J. (2002) Endocytosis: curvature to the ENTH degree. Curr. Biol. 12, R770-772   DOI   ScienceOn
22 Wendland, B. (2002) Epsins: adaptors in endocytosis? Nat. Rev. Mol. Cell Biol. 3, 971-977   DOI   ScienceOn
23 Altenbach, C., Greenhalgh, D. A., Khorana, H. G., and Hubbell, W. L. (1994) A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA 91, 1667-1671   DOI   ScienceOn
24 Chen, H., Fre, S., Slepnev, V. I., Capua, M. R., Takei, K., et al. (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394, 793-797   DOI   ScienceOn
25 Hyman, J., Chen, H., Di Fiore, P. P., De Camilli, P., and Brunger, A. T. (2000) Epsin 1 undergoes nucleocytosolic shuttling and its eps15 interactor NH(2)-terminal homology (ENTH) domain, structurally similar to Armadillo and HEAT repeats, interacts with the transcription factor promyelocytic leukemia Zn(2)+ finger protein (PLZF). J. Cell Biol. 149, 537-546   DOI   ScienceOn
26 Huang, S., Lifshitz, L., Patki-Kamath, V., Tuft, R., Fogarty, K., et al. (2004) Phosphatidylinositol-4,5-bisphosphate-rich plasma membrane patches organize active zones of endocytosis and ruffling in cultured adipocytes. Mol. Cell. Biol. 24, 9102- 9123   DOI   ScienceOn
27 Koshiba, S., Kigawa, T., Kikuchi, A., and Yokoyama, S. (2002) Solution structure of the epsin N-terminal homology (ENTH) domain of human epsin. J. Struct. Funct. Genomics 2, 1-8   DOI   ScienceOn
28 Itoh, T. and Takenawa, T. (2004) Regulation of endocytosis by phosphatidylinositol 4,5-bisphosphate and ENTH proteins. Curr. Top Microbiol. Immunol. 282, 31-47
29 Kirchhausen, T. (2000a) Clathrin. Annu. Rev. Biochem. 69, 699- 727   DOI   ScienceOn
30 Kirchhausen, T. (2000b) Three ways to make a vesicle. Nat. Rev. Mol. Cell. Biol. 1, 187-198   DOI   ScienceOn
31 Russell, C. J., Thorgeirsson, T. E., and Shin, Y. K. (1999) The membrane affinities of the aliphatic amino acid side chains in an alpha-helical context are independent of membrane immersion depth. Biochemistry 38, 337-346   DOI   ScienceOn
32 Ford, M. G., Pearse, B. M., Higgins, M. K., Vallis, Y., Owen, D. J., et al. (2001) Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051-1055   DOI
33 Brodin, L., Low, P., and Shupliakov, O. (2000) Sequential steps in clathrin-mediated synaptic vesicle endocytosis. Curr. Opin. Neurobiol. 10, 312-320   DOI   ScienceOn
34 Shin, Y. K., Levinthal, C., Levinthal, F., and Hubbell, W. L. (1993) Colicin E1 binding to membranes: time-resolved studies of spin-labeled mutants. Science 259, 960-963   DOI
35 Chen, H., Slepnev, V. I., Di Fiore, P. P., and De Camilli, P. (1999) The interaction of epsin and Eps15 with the clathrin adaptor AP-2 is inhibited by mitotic phosphorylation and enhanced by stimulation-dependent dephosphorylation in nerve terminals. J. Biol. Chem. 274, 3257-3260   DOI   ScienceOn
36 Han, X., Bushweller, J. H., Cafiso, D. S., and Tamm, L. K. (2001) Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol. 8, 715-720   DOI   ScienceOn
37 McHaourab, H. S., Lietzow, M. A., Hideg, K., and Hubbell, W. L. (1996) Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry 35, 7692-7704   DOI   ScienceOn